For 20 years, Adrian Owen, a CIFAR senior fellow and co-director of CIFAR’s Azrieli Program in Brain Mind & Consciousness, has been working at the forefront of neuroscience, pushing the boundaries of consciousness research and using the newest technology to communicate with non-responsive victims of traumatic brain injuries. In his new book Into The Gray Zone: A Neuroscientist Explores the Border between Life and Death, Owen tells the story from a new perspective, that of the patients and their families, giving readers insight into what it’s actually like to be in the vegetative state – seemingly unresponsive but potentially still conscious – and sharing the difficulties and triumphs of patients his research has impacted.

N&I: Your book is called “Into the Gray Zone.” What is the gray zone?

AO: Many of the patients that we see and assess appear to be in a vegetative state and turn out to actually be conscious and aware of everything going on around them. That’s really what I mean by “the grey zone.” They’re in a situation where it’s not at all apparent of where they lie on this continuum.

N&I: Can you describe the difference between the vegetative state, being in a coma, and being locked in?

AO: A coma is typically the first thing that happens to you after you have a serious brain injury and you have no wakefulness and typically no sleeping and waking cycles.

A vegetative state often occurs after coma. The person has emerged from a coma and they’ll often have sleeping and waking cycles but won’t respond to any form of external stimulation. This is why vegetative state is often referred to as a state of wakefulness without awareness.

Finally, locked in syndrome, is a very specific clinical condition that leaves patients entirely paralyzed, except for the ability to move their eyes and that usually occurs in the context of completely preserved cognitive function.

N&I: Tell me about the method you’ve created to communicate with patients in the grey zone

AO: In 2006, we published a paper in Science showing that patients who appeared to be entirely non-responsive could respond with their brains. The way we did that was to ask them to imagine a certain scenario that we knew was associated with brain activity in one particular area of the cortex.

The most famous example is that we asked patients to imagine playing a game of tennis because this produces activity in the premotor cortex, the area of your brain that’s involved in setting up sequences of movements and imagining those movements.

Even though the patient could not respond physically, we got them to make a voluntary response with their brain. And once we had a number of these tasks, we were able to ask a patient to do one thing to convey a yes, and a different thing to convey a no.

It was just a proof of principle at that stage. With subsequent patients we’ve gone on to ask things like, “Are you in pain?” “Do you still enjoy listening to this type of music?” That sort of thing.

N&I: Your research shows that about 20 percent of people in a vegetative state are actually in this grey zone with some level of consciousness, but your tests haven’t always been able to detect that consciousness, such as with your patient Juan. How much do we still have to learn here?

The cover of Adrian Owen’s new book, Into the Gray Zone

AO: I think we have a lot to learn. Juan is a complete mystery to me. He’s an incredible patient and I’ve never read of a case like his in the scientific literature. I haven’t had many patients recover from appearing to be entirely vegetative to being able to go back to college. But the really amazing thing about Juan is that he could report his experiences with a high level of accuracy. He could look back and he could say, “Yes, I remember the day you scanned me. I remember you showed me an Alfred Hitchcock film. I remember I was afraid in the scanner.” It’s the absolute evidence that he was conscious because he was actually able to report all of this. We didn’t have to infer consciousness through a brain scan.

Why didn’t we pick that up on the scanner? As I say in the book, this is a mystery. It’s possible that the paths in his brain that were damaged had interfered with the scans. If I ask you to imagine playing tennis you’re going to activate your premotor cortex. If you’re brain damage involves the premotor cortex, you might not activate the premotor cortex, yet, you might still be conscious.

N&I:   At first you looked to solve the problem of communicating with patients who are unable to confirm their consciousness physically, but now you’ve turned to the possibility that patients may not have the cognitive resources to report mentally. How is that different from not being conscious?

AO: Most of the patients who are in this grey zone are actually described as being minimally conscious these days. That means they’re like a vegetative patient, but have the capacity to show some level of awareness at least some of the time. It occurred to me over a number of years that it’s often the case that the minimally conscious patients can’t do things like tennis imagery.

How cognitively demanding a task is can have an effect on our ability to be able to perform in a test but not have any bearing on our consciousness. This is why we turn to other methods like getting people to watch movies.

N&I:   How has your involvement with CIFAR in the past few years contributed to your research?

AO: It has contributed tremendously because it has allowed me to take the clinical elements of the research I do and look at them with a much bigger perspective, in the context of consciousness and what it really means to be human.

One of the things we’ve been exploring with the CIFAR program is What is it that we should be measuring? What is the level of consciousness? How best can we measure it?

We had a whole meeting about the taxonomy of consciousness. Is it the right thing to be talking about memory and attention and executive function as though they were separate things in the brain? In my case, looking at patients with disorders of consciousness indicates that some of these distinctions that we have don’t make much sense when you look at the brain. Can you have really have memory without attention? I don’t think you can. In which case, what’s the point of having two different terms,

N&I:   In the book, you talk about how when you first started seeing these responses from patients, it felt like you were at the beginning of a completely new interface between science and medicine. Where are we terms of that interface now?

AO:     We published a paper earlier this year on a technique known as “Functional Near Infrared Spectroscopy” and this works in a way that’s quite similar to fMRI. It uses light to detect blood-oxygenation levels and detect brain activity. It’s portable, much more cost effective than fMRI, and as effective as fMRI in detecting when somebody’s imagining playing tennis. You could conceivably, not too far from now, imagine sending somebody home with a system like this that would enable them to communicate on a regular basis with their relatives.

The development of fNIRS came out of discussions at one of the early CIFAR meetings where I came back and thought, “I think we could try that and it might just work,” and it did.

N&I: How far are we from making these types of things standard clinical practice and what’s standing in the way of that?

AO: I think the road to widespread clinical usage is typically quite a long one and not just because it isn’t technically possible. There are questions like economics that often come into play.

I would like to make a plea for more widespread use of techniques like fMRI in patient populations like disorders of consciousness. I think both diagnosis and prognosis can be improved by incorporating fMRI into the clinical assessment.

N&I: How have public and practitioner attitudes towards patients in this vegetative state changed since your research came out?

AO: One of the things I really enjoyed about writing the book was it actually opened my eyes up to how far we’ve come over that 20-year period. Views really have changed quite profoundly. Twenty years ago, everybody thought I was completely bonkers putting a vegetative patient into a scanner because it was a waste of money and time because, they thought we weren’t going to see any brain activity, let alone discover that somebody was conscious.

It was only 10 years after that showed that quite a few of these patients are conscious, and just a couple of years after that we started to communicate with patients. When I think about that in the context of the evolution of science and how your understanding of the world can change, it’s amazing.

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